Virulence evolution in the Russian wheat aphid and its impact on Australia’s preparedness strategy

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Virulence evolution in the Russian wheat aphid Owain Edwards | Group Leader, Invertebrate Genomics & Evolution CSIRO ECOSYSTEM SCIENCES, PERTH, WA

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The Problem  Through the GRDC, the Australian grains industry is developing a RWA pre-emptive breeding strategy  History has demonstrated that any widespread deployment of RWA-resistant lines leads to the appearance of resistance-breaking (virulent) biotypes  How can we ensure that resistant lines developed for Australia will be effective against an RWA incursion, and will remain durable?

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Aims  To understand the mechanisms of virulence evolution in RWA, and  To use this information to inform the RWA preemptive breeding program to assist in the breeding of RWA-resistant lines

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RWA recent history  Evidence for a host shift to cereals in last 10,000 years - all RWA worldwide can be traced back to a single mitochondrial haplotype (Bo Zhang’s CRCNPB PhD project)

 Virulent biotypes are closely related to virulent biotypes in same area

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RWA damage symptoms  Leaf rolling  Chlorosis  Biomass reduction

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Aphid Feeding

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Aphid salivary genomics  Aphid salivary proteins are somehow evolving faster than their homologues in other insects  Most often achieved through gene duplication and diversifying selection

IAGC 2010. PLoS Biology Carolan et al. 2011. J. Proteom. Res.

ACYPI000001 ACYPI006675 ACYPI000734 ACYPI008967 ACYPI001389 ACYPI003280 ACYPI003669

ACYPI001227 ACYPI001092 ACYPI007583 ACYPI002583 ACYPI003165 ACYPI005810 ACYPI010198 ACYPI009427 ACYPI004403

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Aphid salivary transcriptomics  High levels of transcript diversity in salivary gland genes  Transcripts all related to the same pea aphid orthologue, suggesting they are alleles of the same gene rather than arising from gene duplicates  Transcriptional infidelity?

Cui et al. 2012. Insect Science

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Virulence phenotypes  Leaf rolling always proportional to aphid population growth  Chlorosis can be independent of leaf rolling (and aphid numbers) 350

3.5 Aphid Numbers

300

10

Leaf Rolling

Chlorosis

3.0 8

250

2.5

200

2.0

150

1.5

100

1.0

Jimoh et al, 2011. Ent Exp Appl

6

4

2 50

0.5

0

0.0 SA1

SA2

0 SA1

SA2

SA1

SA2

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Virulence phenotypes  Virulence phenotype often varies with host plant  “Hypervirulence” phenotype: excessive chlorosis Leaf rolling

Chlorosis

0.8

Wheat

1.0

Barley

Wheat

Barley

Fraction of plants

Resistant Susceptible

0.4

Fraction of plants

0.8

0.6

Resistant Susceptible 0.6

0.4

0.2 0.2

0.0

0.0

Mexico

Hungary

Mexico

Hungary

Mexico

Edwards et al., in prep

Hungary

Mexico

Hungary

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Summary  Rapid evolution of salivary gland genes allows RWA to quickly develop resistance-breaking virulent biotypes  Leaf rolling and chlorosis are independent damage symptoms, and can depend on the host plant o Leaf rolling is adaptive, associated with aphid population growth o Chlorosis is maladaptive, perhaps a reflection of the novel host association with cereals

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Ongoing research  RNASeq (transcriptome) comparisons of biotypes o “virulence” comparisons (population growth/leaf rolling) o “hypervirulence” comparisons (chlorosis)  Assisting the Australian and global RWA breeding efforts o demonstrating the need to measure all symptoms (because they are independent) o providing access to both “virulent” and “hypervirulent” biotypes at CSIRO’s European Laboratory

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Acknowledgements Jerry Reeck, John Reese, Mike Smith Jim Carolan, Tom Wilkinson Ted Botha Feng Cui, Le Kang

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